Collective decision-making in honey bees: how colonies choose among nectar sources

Summary A honey bee colony can skillfully choose among nectar sources. It will selectively exploit the most profitable source in an array and will rapidly shift its foraging efforts following changes in the array. How does this colony-level ability emerge from the behavior of individual bees? The answer lies in understanding how bees modulate their colony's rates of recruitment and abandonment for nectar sources in accordance with the profitability of each source. A forager modulates its behavior in relation to nectar source profitability: as profitability increases, the tempo of foraging increases, the intensity of dancing increases, and the probability of abandoning the source decreases. How does a forager assess the profitability of its nectar source? Bees accomplish this without making comparisons among nectar sources. Neither do the foragers compare different nectar sources to determine the relative profitability of any one source, nor do the food storers compare different nectar loads and indicate the relative profitability of each load to the foragers. Instead, each forager knows only about its particular nectar source and independently calculates the absolute profitability of its source. Even though each of a colony's foragers operates with extremely limited information about the colony's food sources, together they will generate a coherent colonylevel response to different food sources in which better ones are heavily exploited and poorer ones are abandoned. This is shown by a computer simulation of nectar-source selection by a colony in which foragers behave as described above. Nectar-source selection by honey bee colonies is a process of natural selection among alternative nectar sources as foragers from more profitable sources survive (continue visiting their source) longer and reproduce (recruit other foragers) better than do foragers from less profitable sources. Hence this colonial decision-making is based on decentralized control. We suggest that honey bee colonies possess decentralized decision-making because it combines effectiveness with simplicity of communication and computation within a colony. Offprint requests to: T.D. Seeley     

Social foraging in honey bees: how nectar foragers assess their colony's nutritional status

Summary A honey bee colony operates as a tightly integrated unit of behavioral action. One manifestation of this in the context of foraging is a colony's ability to adjust its selectivity among nectar sources in relation to its nutritional status. When a colony's food situation is good, it exploits only highly profitable patches of flowers, but when its situation is poor, a colony's foragers will exploit both highly profitable and less profitable flower patches. The nectar foragers in a colony acquire information about their colony's nutritional status by noting the difficulty of finding food storer bees to receive their nectar, rather than by evaluating directly the variables determining their colony's food situation: rate of nectar intake and amount of empty storage comb. (The food storer bees in a colony are the bees that collect nectar from returning foragers and store it in the honey combs. They are the age group (generally 12–18 day old bees) that is older than the nurse bees but younger than the foragers. Food storers make up approximately 20% of a colony members.) The mathematical theory for the behavior of queues indicates that the waiting time experienced by nectar foragers before unloading to food storers (queue length) is a reliable and sensitive indicator of a colony's nutritional status. Queue length is automatically determined by the ratio of two rates which are directly related to a colony's nutritional condition: the rate of arrival of loaded nectar foragers at the hive (arrival rate) and the rate of arrival of empty food storers at the nectar delivery area (service rate). These two rates are a function of the colony's nectar intake rate and its empty comb area, respectively. Although waiting time conveys crucial information about the colony's nutritional status, it has not been molded by natural selection to serve this purpose. Unlike signals, which are evolved specifically to convey information, this cue conveys information as an automatic by-product. Such cues may prove more important than signals in colony integration.     

Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive

Food quality is a relevant characteristic to be transferred within eusocial insect colonies because its evaluation improves the collective foraging efficiency. In honeybees, colony mates could directly acquire this resource characteristic during trophallactic encounters with nectar foragers. In the present study, we focused on the gustatory responsiveness of bees that have unloaded food from incoming foragers. The sugar sensitivity of receiver bees was assessed in the laboratory by using the proboscis extension response paradigm. After unloading, hive bees were captured either from a colony that foraged freely in the environmental surroundings or from a colony that foraged at an artificial feeder with a known sucrose solution. In the first situation, the sugar sensitivity of the hive bees negatively correlated with the sugar concentration of the nectar crops brought back by forager mates. Similarly, in the controlled situation, the highest sucrose concentration the receivers accepted during trophallaxis corresponded to the highest thresholds to sucrose. The results indicate that first-order receivers modify their sugar sensitivity according to the quality of the food previously transferred through trophallaxis by the incoming foragers. In addition, trophallaxis is a mechanism capable of transferring gustatory information in honeybees. Its implications at a social scale might involve changes in the social information as well as in nectar distribution within the colony.     

Why do honey-bee (Apis millifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system

The task of nectar foraging in honey-bees is partitioned between foragers and receivers. Foragers typically transfer a nectar load in the nest as sub-loads to several receivers rather than as a single transfer. Foragers experience delays in finding receivers and use these delays to balance the number of foragers and receivers. A short delay results in the forager-recruiting waggle dance whereas a long delay results in the receiver-recruiting tremble dance. Several nectar transfers increase the cost of this system by introducing additional delays in finding extra receivers. We tested four hypotheses to explain the occurrence of multiple transfer. We found no evidence that multiple transfer is due to different crop capacities of foragers and receivers or that it results from extensive trophallactic interactions with nest-mates. Receiver bees frequently evaporate nectar in their mouthparts to hasten the production of honey. The suggestion has been made that multiple transfer is driven by receivers who take partial loads from foragers to enhance nectar evaporation. An alternative suggestion is that foragers drive multiple transfer to gain better information on the balance of foragers and receivers. Multiple sampling of the delay in finding a receiver reduces the standard deviation of the delay mean and so provides foragers with better information than is provided by a single delay. The enhanced-evaporation hypothesis predicts that receivers break foragers' first transfer whereas the information improvement hypothesis predicts foragers break their first transfers. Furthermore, only the information improvement hypothesis predicts a high level of multiple receptions. Data on transfer break-off and receiver behaviour strongly support the information improvement hypothesis and reject the enhanced-evaporation hypothesis. We suggest that multiple transfer is an adaptive sampling mechanism, which improves foragers' information on colony work allocation, and that multiple sampling is a common feature of social insect societies.     

The tremble dance of the honey bee: message and meanings

Summary The nectar foragers of a honey bee colony, upon return to the hive, sometimes perform a mysterious behavior called the tremble dance. In performing this dance, a forager shakes her body back and forth, at the same time rotating her body axis by about 50° every second or so, all the while walking slowly across the comb. During the course of a dance, which on average lasts 30 min, the bee travels about the broodnest portion of the hive. It is shown experimentally that a forager will reliably perform this dance if she visits a highly profitable nectar source but upon return to the hive experiences great difficulty finding a food-storer bee to take her nectar. This suggests that the message of the tremble dance is I have visited a rich nectar source worthy of greater exploitation, but already we have more nectar coming into the hive than we can handle. It is also shown experimentally that the performance of tremble dances is followed quickly by a rise in a colony's nectar processing capacity and (see Nieh, in press and Kirchner, submitted) by a drop in a colony's recruitment of additional bees to nectar sources. These findings suggest that the tremble dance has multiple meanings. For bees working inside the hive, its meaning is apparently I should switch to the task of processing nectar, while for bees working outside the hive (gathering nectar), its meaning is apparently I should refrain from recruiting additional foragers to my nectar source. Hence it appears that the tremble dance functions as a mechanism for keeping a colony's nectar processing rate matched with its nectar intake rate at times of greatly increased nectar influx. Evidently the tremble dance restores this match in part by stimulating a rise in the processing rate, and in part by inhibiting any further rise in the intake rate. Correspondence to: T. Seeley     

Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications

The return of a successful bumblebee forager stimulates nestmates to leave the nest and search for food. Here we investigate the mechanisms by which this happens. Successful Bombus terrestris foragers perform irregular runs in their nest, often lasting for several minutes. Run duration is at its maximum when food has just been discovered. Running likely serves to distribute a pheromone, since the information flow between "runners" and "recruits" can be disrupted by eliminating air exchange, while leaving other potential means of communication intact. In addition, nectar stores in the nest may be monitored continuously. A sudden influx of nectar into the nest also causes measurable increases in forager activity. The implications of bumblebee recruitment behavior for the evolution of communication in bees are discussed.     

Manuscript in preparation for <Emphasis Type="Italic">Behavioral Ecology and Sociobiology</Emphasis> Bumble bee pollen foraging regulation: role of pollen quality,storage levels,and odor

The regulation of protein collection through pollen foraging plays an important role in pollination and in the life of bee colonies that adjust their foraging to natural variation in pollen protein quality and temporal availability. Bumble bees occupy a wide range of habitats from the Nearctic to the Tropics in which they play an important role as pollinators. However, little is known about how a bumble bee colony regulates pollen collection. We manipulated protein quality and colony pollen stores in lab-reared colonies of the native North American bumble bee, Bombus impatiens. We debut evidence that bumble bee colony foraging levels and pollen storage behavior are tuned to the protein quality (range tested: 17–30% protein by dry mass) of pollen collected by foragers and to the amount of stored pollen inside the colony. Pollen foraging levels (number of bees exiting the nest) significantly increased by 55%, and the frequency with which foragers stored pollen in pots significantly increased by 233% for pollen with higher compared to lower protein quality. The number of foragers exiting the nest significantly decreased (by 28%) when we added one pollen load equivalent each 5 min to already high intranidal pollen stores. In addition, pollen odor pumped into the nest is sufficient to increase the number of exiting foragers by 27%. Foragers directly inspected pollen pots at a constant rate over 24 h, presumably to assess pollen levels. Thus, pollen stores can act as an information center regulating colony-level foraging according to pollen protein quality and colony need. An erratum to this article can be found at     

Exploitation of carbohydrate food sources in <Emphasis Type="Italic">Polybia occidentalis</Emphasis>: social cues influence foraging decisions in swarm-founding wasps

An efficient exploitation of carbohydrate food sources would be beneficial for social wasp species that store nectar within their nest. In the swarm-founding polistine wasp Polybia occidentalis, we now demonstrate that the decisions of when and where to forage are influenced by information from conspecifics. Only when foragers had been trained to collect at artificial carbohydrate feeders did newcomers (food-source-naive individuals) continuously arrive at these feeders during 2 h of experiment. In control tests, in which no forager had been trained, not a single newcomer alighted at any of the offered carbohydrate food sources. This indicates that, during the foraging process, a nest-based input provided by successful foragers must have stimulated nestmates to search for food. Once activated, the newcomers’ choice on where to collect was strongly influenced by field-based social information. The mere visual presence of accumulated conspecifics (wasp dummies placed on one of the feeders) attracted newcomers to the food sources. Interestingly, however, visual enhancement was not the only decision-biasing factor at the feeding site. In an experimental series where searching wasps had to choose between the experimental feeder at which 3 foragers continuously collected and the control feeder with nine wasp dummies, only 40% of the wasps chose the visually enhanced feeder. This points to the existence of additional mechanisms of local enhancement. The possibility that, in social wasps, recruitment is involved in the exploitation of carbohydrate food sources is discussed.     

Look before you leap: is risk of injury a foraging cost?

Theory states that an optimal forager should exploit a patch so long as its harvest rate of resources from the patch exceeds its energetic, predation, and missed opportunity costs for foraging. However, for many foragers, predation is not the only source of danger they face while foraging. Foragers also face the risk of injuring themselves. To test whether risk of injury gives rise to a foraging cost, we offered red foxes pairs of depletable resource patches in which they experienced diminishing returns. The resource patches were identical in all respects, save for the risk of injury. In response, the foxes exploited the safe patches more intensively. They foraged for a longer time and also removed more food (i.e., had lower giving up densities) in the safe patches compared to the risky patches. Although they never sustained injury, video footage revealed that the foxes used greater care while foraging from the risky patches and removed food at a slower rate. Furthermore, an increase in their hunger state led foxes to allocate more time to foraging from the risky patches, thereby exposing themselves to higher risks. Our results suggest that foxes treat risk of injury as a foraging cost and use time allocation and daring—the willingness to risk injury—as tools for managing their risk of injury while foraging. This is the first study, to our knowledge, which explicitly tests and shows that risk of injury is indeed a foraging cost. While nearly all foragers may face an injury cost of foraging, we suggest that this cost will be largest and most important for predators.     

A stingless bee (Melipona panamica) indicates food location without using a scent trail

The study of location specification in recruitment communication by bees has focused on two dimensions: direction and distance from the nest. Yet the third dimension, height above ground, may be significant in the tall and dense forest habitats of stingless bees. Foragers of the stingless bee Scaptotrigona postica recruit to a specific three-dimensional location by laying a scent trail. Stingless bees in the genus Melipona are thought to have a more sophisticated recruitment system that communicates distance through sounds inside the nest and direction through pointing zig-zag flights outside the nest. However, prior research on Melipona has not examined height communication or even established that foragers can recruit newcomers to a specific location. We used identical paired feeders to investigate recruitment to food in M panamica on Barro Colorado Island, Panama. We trained foragers from an observation hive to one feeder and monitored both feeders for the subsequent arrival of newcomers. We changed the relative positions of the feeders to test for correct direction, distance, and canopy-level communication. A 40-m canopy tower located inside the forest enabled us to examine canopy-level communication. We found that M. panamica foragers can recruit to a specific (1) direction, (2) distance, and (3) canopy level. To test the possibility that foragers accomplish this by means of a scent trail, we placed the colony on one shore of a small cove and trained bees over 116 m of open water to a feeder located on the opposite shore. We also placed a second feeder on this shore, equidistant from the colony but 20 m from the first feeder. Significantly more newcomers consistently arrived at the feeder visited by the foragers. Thus foragers evidently do not need a scent trail to communicate direction. Inside the nest, a forager produces pulsed sounds while visibly vibrating her wings after returning from a good food source. She is attended by other bees who cluster and hold their antennae around her, following her as she rapidly spins clockwise and counterclockwise. Locational information may be encoded in this behavior. However, foragers may also directly lead newcomers to the food source. Further experiments are planned to test for such piloting and other communication mechanisms.     

The control of water collection in honey bee colonies

A honey bee (Apis mellifera) colony adaptively controls the collection of water by its foragers, increasing it when high temperatures necesssitate evaporative cooling inside the hive and decreasing it when the danger of overheating passes. This study analyzes the mechanisms controlling water collection once it has begun, that is, how a colony's water collectors know whether to continue or stop their activity. M. Lindauer suggested that water collectors acquire information about their colony's need for more water by noting how easily they can unload their water to bees inside the hive. In support of this hypothesis, we found that a water collector's ease of unloading does indeed change when her colony's need for water changes. How does a water collector sense the ease of unloading? Multiple variables of the unloading experience change in relation to a colony's water need. Three time-based variables – initial search time, total search time, and delivery time – all change quite strongly. But what changes most strongly is the number of unloading rejections (refusals by receiver bees to take the water), suggesting that this is the primary index of ease of unloading. Why does a water collector's ease of unloading change when her colony's need for water changes? Evidently, what links these two variables is change in the number of water receivers. These are middle-aged bees that receive water just inside the hive entrance, then transport it deeper inside the hive, and finally smear it on the walls of cells or give it to other bees, or both. A colony increases the number of water receivers when its water need increases by having bees engaged in nectar reception and other tasks (and possibly also bees that are not working) switch to the task of water reception. Evidently the activation of additional water receivers does not strongly reduce the number of nectar receivers in a colony, since a colony can increase greatly its water collection without simultaneously decreasing its collection of rich nectar. This study provides a clear example of the way that the members of a social insect colony can use indirect indicators of their colony's labor needs to adaptively control the work that they perform.     

Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera : Vespidae)

We measured patterns of individual forager specialization and colony-wide rates of material input during periods of response to experimental nest damage and during control periods in three colonies of the tropical social wasp Polybia occidentalis.

Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. Received: 8 December 1997 / Accepted after revision: 28 March 1998     

Food-exchange by foragers in the hive – a means of communication among honey bees?

Dancing and trophallactic behaviour of forager honey bees, Apis mellifera ligustica >Spinola, that returned from an automatic feeder with a regulated flow rate of 50% weight-to-weight sucrose solution (range: 0.76–7.65 μl/min) were studied in an observation hive. Behavioural parameters of dancing, such as probability, duration and dance tempo, increased with the nectar flow rate, though with very different response curves among bees. For trophallaxis (i.e. mouth-to-mouth exchange of food), the frequency of giving-contacts and the transfer rate of the nectar increased with the nectar flow rate. After unloading, foragers often approached other nest mates and begged for food before returning to the food source. This behaviour was less frequent at higher nectar flow rates. These results show that the profitability of a food source in terms of nectar flow rate had a quantitative representation in the hive through quantitative changes in trophallactic and dancing behaviour. The role of trophallaxis as a communication channel during recruitment is discussed. Received: 14 January 1995/Accepted after revision: 14 August 1995     

The occurrence and context of tremble dancing in free-foraging honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Nectar foraging in honey bees is regulated by several communication signals that are performed mainly by foragers. One of these signals is the tremble dance, which is consistently performed by foragers from a rich food source which, upon return to the hive, experience a long delay before unloading their nectar to a nectar receiver. Although tremble dancing has been studied extensively using artificial nectar sources, its occurrence and context in a more natural setting remain unknown. Therefore, this study tests the sufficiency of the current explanations for tremble dancing by free-foraging honey bees. The main finding is that only about half of the observations of tremble dancing, referred to as delay-type tremble dancing, are a result of difficulty in finding a nectar receiver. In the remaining observations, tremble dancing was initiated immediately upon entering the hive, referred to as non-delay-type tremble dancing. Non-delay tremble dancing was associated with first foraging successes, both in a forager's career and in a single day. More than 75% of tremble dancing was associated with good foraging conditions, as indicated by the dancer continuing to forage after dancing. However, at least some of the other cases were associated with deteriorated foraging conditions, such as the end of the day, after which foraging was discontinued. No common context could be identified that explains all cases of tremble dancing or the subset of non-delay-type tremble dancing. This study shows that the current explanations for the cause of the tremble dance are insufficient to explain all tremble dancing in honey bees that forage at natural food sources.     

Recruitment to food by the German yellowjacket, Vespula germanica

The hypothesis that Vespula germanica foragers can recruit nestmates to food resources was tested using a protocol that controlled for the biasing effects of social factors at the resource, including local enhancement and food-site marking substances. Foragers from an observation colony in the field were trained to visit a dish of scented corn syrup solution 15?m east of the nest. A second feeding station, 22?m northeast of the nest, offered incoming foragers a choice between food with the training scent and food with a control scent. Significantly more naive foragers arriving at that station chose the food with the training scent. We conclude that the German yellowjacket is able to recruit nestmates to carbohydrate food sources, and that recruits use food odor to locate the source of food being brought into the nest.     

Nest defense and central place foraging: A model and experiment

Summary A graphical model presented here indicates that a nest-defending forager should stay closer to its nest, forage for shorter times per patch, and deliver smaller loads than predicated for delivery rate maximization. The effect is more pronounced farther from the nest, so that if nest defense is especially important, the predator should leave far patches sooner than near ones, and deliver smaller loads from farther away. Moreover, if the attack rate at the nest is increased, the defending forager should move closer and deliver smaller prey.Experimental attacks with stuffed specimens at Gila woodpecker (Melanerpes uropygialis) nests produced the predicted changes in the foraging behavior of males, but not of females.Mated pairs may work as a team to pursue simultaneously two conflicting goals—food delivery and nest protection—both of which affect the survivorship of the young. Sexual dimorphism in monogamous species may result in part from specialization in these roles.     

Ideal free distributions under predation risk

 We examine the trade-off between gathering food and avoiding predation in the context of patch use by a group of animals. Often a forager will have to choose between feeding sites that differ in both energetic gain rate and predation risk. The ideal site will have a high gain rate and low risk of predation. However, intake rate will often decrease when the patch is shared with other foragers and it may be optimal for some individuals to feed elsewhere. Within the framework of ideal free theory, we investigate the distribution of foragers that will equalise individual fitness gains. We focus on a two-patch environment with continuous inputs of food. With reference to existing experimental studies, we examine the effects of risk dilution, food input rates and an animal’s expectations of the future. We identify the effect of total animal numbers when one patch is subject to predation risk and the other is safe. Conditions under which the difference in intake rate in the two patches is constant are identified, as are conditions in which the ratio of animals in the two patches is constant. If current conditions do not alter future expectations an increase in input rates to the patches promotes increased use of the risky patch. Yet, if conditions are assumed to persist indefinitely the opposite effect is seen. When both patches are subject to predation risk, dilution of risk favours more extreme distributions, and may lead to more than one stable distribution. The results of these models are used to critically analyse previous work on the energetic equivalence of risk. This paper is intended to help guide the development of new experimental studies into the energy-risk trade-off. Received: 10 February 1995/Accepted after revision: 1 October 1995     

Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept

Social insect colonies need to explore and exploit multiple food sources simultaneously and efficiently. At the individual level, this colony-level behaviour has been thought to be taken care of by two types of individual: scouts that independently search for food, and recruits that are directed by nest mates to a food source. However, recent analyses show that this strict division of labour between scouts and recruits is untenable. Therefore, a modified concept is presented here that comprises the possible behavioural states of an individual forager (novice forager, scout, recruit, employed forager, unemployed experienced forager, inspector and reactivated forager) and the transitions between them. The available empirical data are reviewed in the light of both the old and the new concept, and probabilities for the different transitions are derived for the case of the honey-bee. The modified concept distinguishes three types of foragers that may be involved in the exploration behaviour of the colony: novice bees that become scouts, unemployed experienced bees that scout, and lost recruits, i.e. bees that discover a food source other than the one to which they were directed to by their nest mates. An advantage of the modified concept is that it allows for a better comparison of studies investigating the different roles performed by social insect foragers during their individual foraging histories. Received: 29 December 1999 / Revised: 25 February 2000 / Accepted: 16 October 2000